The PGC-1 coactivators promote an anti-inflammatory environment in skeletal muscle in vivo

Biochemical and Biophysical Research Communications

Volumn 464, Issue 3, 2015, Pages 692-697

  Eisele, Petra Sabine ^a,b   Furrer, Regula ^a   Beer, Markus ^a   Handschin, Christoph ^a,b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Inflammation; Metabolism; Mitochondria; PGC 1; Skeletal muscle

Indexed keywords

CCL1 CHEMOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 12; INTERLEUKIN 6; MACROPHAGE DERIVED CHEMOKINE; OSTEOPONTIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CYTOKINE; LIPOPOLYSACCHARIDE; PPARGC1A PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IN VIVO STUDY; INFLAMMATION; MACROPHAGE; MALE; MOUSE; MUSCLE CELL; MUSCLE FUNCTION; MUSCLE TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; ANIMAL; C57BL MOUSE; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

ANIMALS; CYTOKINES; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-12; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SKELETAL; NF-KAPPA B; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84938748358     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2015.06.166     Document Type: Article

References (32)

1. M.C. Arkan, A.L. Hevener, F.R. Greten, S. Maeda, Z.W. Li, J.M. Long, A. Wynshaw-Boris, G. Poli, J. Olefsky, and M. Karin IKK-beta links inflammation to obesity-induced insulin resistance Nat. Med. 11 2005 191 198
2. G.S. Hotamisligil, N.S. Shargill, and B.M. Spiegelman Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance Science 259 1993 87 91
3. C.N. Lumeng, S.M. Deyoung, J.L. Bodzin, and A.R. Saltiel Increased inflammatory properties of adipose tissue macrophages recruited during diet-induced obesity Diabetes 56 2007 16 23
4. S.P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R.L. Leibel, and A.W. Ferrante Jr. Obesity is associated with macrophage accumulation in adipose tissue J. Clin. Invest. 112 2003 1796 1808
5. S.K. Biswas, and A. Mantovani Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm Nat. Immunol. 11 2010 889 896
6. J.M. Olefsky, and C.K. Glass Macrophages, inflammation, and insulin resistance Annu Rev. Physiol. 72 2010 219 246
7. M. Gleeson Immune function in sport and exercise J. Appl. Physiol. 103 2007 693 699
8. W.C. Knowler, E. Barrett-Connor, S.E. Fowler, R.F. Hamman, J.M. Lachin, E.A. Walker, and D.M. Nathan Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin N. Engl. J. Med. 346 2002 393 403
9. M.C. Chan, and Z. Arany The many roles of PGC-1alpha in muscle-recent developments Metabolism 63 2014 441 451
10. C. Handschin, and B.M. Spiegelman The role of exercise and PGC1alpha in inflammation and chronic disease Nature 454 2008 463 469
11. P. Puigserver, G. Adelmant, Z. Wu, M. Fan, J. Xu, B. O'Malley, and B.M. Spiegelman Activation of PPARgamma coactivator-1 through transcription factor docking Science 286 1999 1368 1371
12. Z. Wu, P. Puigserver, U. Andersson, C. Zhang, G. Adelmant, V. Mootha, A. Troy, S. Cinti, B. Lowell, R.C. Scarpulla, and B.M. Spiegelman Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1 Cell 98 1999 115 124
13. J.A. Calvo, T.G. Daniels, X. Wang, A. Paul, J. Lin, B.M. Spiegelman, S.C. Stevenson, and S.M. Rangwala Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake J. Appl. Physiol. 104 2008 1304 1312
14. J. Lin, H. Wu, P.T. Tarr, C.Y. Zhang, Z. Wu, O. Boss, L.F. Michael, P. Puigserver, E. Isotani, E.N. Olson, B.B. Lowell, R. Bassel-Duby, and B.M. Spiegelman Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres Nature 418 2002 797 801
15. Z. Arany, N. Lebrasseur, C. Morris, E. Smith, W. Yang, Y. Ma, S. Chin, and B.M. Spiegelman The transcriptional coactivator PGC-1beta drives the formation of oxidative type IIX fibers in skeletal muscle Cell. Metab. 5 2007 35 46
16. C. Handschin, S. Chin, P. Li, F. Liu, E. Maratos-Flier, N.K. Lebrasseur, Z. Yan, and B.M. Spiegelman Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals J. Biol. Chem. 282 2007 30014 30021
17. C. Zechner, L. Lai, J.F. Zechner, T. Geng, Z. Yan, J.W. Rumsey, D. Collia, Z. Chen, D.F. Wozniak, T.C. Leone, and D.P. Kelly Total skeletal muscle PGC-1 deficiency uncouples mitochondrial derangements from fiber type determination and insulin sensitivity Cell. Metab. 12 2010 633 642
18. V.K. Mootha, C.M. Lindgren, K.F. Eriksson, A. Subramanian, S. Sihag, J. Lehar, P. Puigserver, E. Carlsson, M. Ridderstrale, E. Laurila, N. Houstis, M.J. Daly, N. Patterson, J.P. Mesirov, T.R. Golub, P. Tamayo, B. Spiegelman, E.S. Lander, J.N. Hirschhorn, D. Altshuler, and L.C. Groop PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes Nat. Genet. 34 2003 267 273
19. M.E. Patti, A.J. Butte, S. Crunkhorn, K. Cusi, R. Berria, S. Kashyap, Y. Miyazaki, I. Kohane, M. Costello, R. Saccone, E.J. Landaker, A.B. Goldfine, E. Mun, R. DeFronzo, J. Finlayson, C.R. Kahn, and L.J. Mandarino Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1 Proc. Natl. Acad. Sci. U. S. A. 100 2003 8466 8471
20. C. Handschin, C.S. Choi, S. Chin, S. Kim, D. Kawamori, A.J. Kurpad, N. Neubauer, J. Hu, V.K. Mootha, Y.B. Kim, R.N. Kulkarni, G.I. Shulman, and B.M. Spiegelman Abnormal glucose homeostasis in skeletal muscle-specific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk J. Clin. Invest. 117 2007 3463 3474
21. P.S. Eisele, S. Salatino, J. Sobek, M.O. Hottiger, and C. Handschin The PGC-1 coactivators repress the transcriptional activity of NF-kappaB in skeletal muscle cells J. Biol. Chem. 288 4 2013 2246 2260
22. A.H. Remels, H.R. Gosker, J. Bakker, D.C. Guttridge, A.M. Schols, and R.C. Langen Regulation of skeletal muscle oxidative phenotype by classical NF-kappaB signalling Biochim. Biophys. Acta 1832 2013 1313 1325
23. K.R. Bastos, J.M. Alvarez, C.R. Marinho, L.V. Rizzo, and M.R. Lima Macrophages from IL-12p40-deficient mice have a bias toward the M2 activation profile J. Leukoc. Biol. 71 2002 271 278
24. J. Magram, S.E. Connaughton, R.R. Warrier, D.M. Carvajal, C.Y. Wu, J. Ferrante, C. Stewart, U. Sarmiento, D.A. Faherty, and M.K. Gately IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses Immunity 4 1996 471 481
25. J. Olesen, S. Larsson, N. Iversen, S. Yousafzai, Y. Hellsten, and H. Pilegaard Skeletal muscle PGC-1alpha is required for maintaining an acute LPS-induced TNFalpha response PLoS One 7 2012 e32222
26. C. Handschin The biology of PGC-1alpha and its therapeutic potential Trends Pharmacol. Sci. 30 2009 322 329
27. C. Handschin, Y.M. Kobayashi, S. Chin, P. Seale, K.P. Campbell, and B.M. Spiegelman PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy Genes. Dev. 21 2007 770 783
28. M.C. Chan, G.C. Rowe, S. Raghuram, I.S. Patten, C. Farrell, and Z. Arany Post-natal induction of PGC-1alpha protects against severe muscle dystrophy independently of utrophin Skelet. Muscle 4 2014 2
29. S.A. Villalta, B. Deng, C. Rinaldi, M. Wehling-Henricks, and J.G. Tidball IFN-gamma promotes muscle damage in the mdx mouse model of Duchenne muscular dystrophy by suppressing M2 macrophage activation and inhibiting muscle cell proliferation J. Immunol. 187 2011 5419 5428
30. S.A. Villalta, C. Rinaldi, B. Deng, G. Liu, B. Fedor, and J.G. Tidball Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype Hum. Mol. Genet. 20 2010 790 805
31. G.C. Rowe, S. Raghuram, C. Jang, J.A. Nagy, I.S. Patten, A. Goyal, M.C. Chan, L.X. Liu, A. Jiang, K.C. Spokes, D. Beeler, H. Dvorak, W.C. Aird, and Z. Arany PGC-1alpha induces SPP1 to activate macrophages and orchestrate functional angiogenesis in skeletal muscle Circulation Res. 115 2014 504 517
32. R.R. Rao, J.Z. Long, J.P. White, K.J. Svensson, J. Lou, I. Lokurkar, M.P. Jedrychowski, J.L. Ruas, C.D. Wrann, J.C. Lo, D.M. Camera, J. Lachey, S. Gygi, J. Seehra, J.A. Hawley, and B.M. Spiegelman Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis Cell 157 2014 1279 1291